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Published online 1 December 2003. doi:10.1083/jcb.200303060
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© The Rockefeller University Press, 0021-9525/2003/12/1077 $8.00
The Journal of Cell Biology, Volume 163, Number 5, 1077-1088

Article

 L1-dependent neuritogenesis involves ankyrinB that mediates L1-CAM coupling with retrograde actin flow

Kazunari Nishimura1, Fumie Yoshihara1, Takuro Tojima1,2, Noriko Ooashi1, Woohyun Yoon3, Katsuhiko Mikoshiba2, Vann Bennett3 and Hiroyuki Kamiguchi1

1 Laboratory for Neuronal Growth Mechanisms, Brain Science Institute, Institute of Physical and Chemical Research (RIKEN), Saitama 351-0198, Japan
2 Division of Molecular Neurobiology, The Institute of Medical Science, The University of Tokyo, Tokyo 108-8639, Japan
3 Howard Hughes Medical Institute and Departments of Cell Biology and Biochemistry, Duke University Medical Center, Durham, NC 27710

Address correspondence to Hiroyuki Kamiguchi, Laboratory for Neuronal Growth Mechanisms, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan. Tel.: 81-48-467-6137. Fax: 81-48-467-9795. email: kamiguchi{at}brain.riken.jp

The cell adhesion molecule L1 (L1-CAM) plays critical roles in neurite growth. Its cytoplasmic domain (L1CD) binds to ankyrins that associate with the spectrin–actin network. This paper demonstrates that L1-CAM interactions with ankyrinB (but not with ankyrinG) are involved in the initial formation of neurites. In the membranous protrusions surrounding the soma before neuritogenesis, filamentous actin (F-actin) and ankyrinB continuously move toward the soma (retrograde flow). Bead-tracking experiments show that ankyrinB mediates L1-CAM coupling with retrograde F-actin flow in these perisomatic structures. Ligation of the L1-CAM ectodomain by an immobile substrate induces L1CD–ankyrinB binding and the formation of stationary ankyrinB clusters. Neurite initiation preferentially occurs at the site of these clusters. In contrast, ankyrinB is involved neither in L1-CAM coupling with F-actin flow in growth cones nor in L1-based neurite elongation. Our results indicate that ankyrinB promotes neurite initiation by acting as a component of the clutch module that transmits traction force generated by F-actin flow to the extracellular substrate via L1-CAM.

Key Words: ankyrin; L1-CAM; adhesion; neurite; clutch

The online version of this article includes supplemental material.

Abbreviations used in this paper: CAM, cell adhesion molecule; DIC, differential interference contrast; DRG, dorsal root ganglion; FRET, fluorescent resonance energy transfer; FRETE, FRET efficiency; L1-CAM, cell adhesion molecule L1; L1CD, L1-CAM cytoplasmic domain; L1ED, L1-CAM extracellular domain.


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